The experience of being a caregiver of patients with digestive cancer, from patients and caregivers’ perception: A mixed study

Backgrounds Caregivers are essential in the care of a patient with digestive cancer. Considering their experience and needs is crucial. Objectives To explore the experience of caregivers of patients with digestive cancer and to compare the perspectives of patients and caregivers. Methods A mixed-methods study with a cross-sectional prospective and a comprehensive qualitative dimension was performed in a medical oncology unit in a French tertiary hospital. Dyads made of patients with digestive cancer and their caregiver were recruited. The Caregiver Reaction Assessment (CRA) and the Supportive Care Needs Survey for Partners and Caregivers (SCNS-PC) questionnaires were distributed to caregivers. The CRA was used to measure the caregiver burden and the SCNS-PC was used to identify the unmet supportive care needs of caregivers. Semi-structured interviews with the dyads were conducted. Qualitative interviews addressed various dimensions of the caregiver’s experience from each dyad’s member perspective. Results Thirty-two caregivers completed the questionnaires. Responses showed high self-esteem, schedule burden, and a need for care and information services. Ten dyads participated in the interviews. Three themes emerged from the caregiver’s interviews: illness is an upheaval; loneliness and helplessness are experienced; caring is a natural role with positive outcomes. Four themes emerged from patient’s interviews: the caregiver naturally assumes the role and gets closer; he is the patient’s anchor; his life is disrupted; anxiety and guilt accompany the desire to protect him. In comparing patient and caregiver data, the main theme of disagreement was their relationship. Conclusions Caregiver care does not appear to be optimal, particularly in terms of their need for information. Patients have a fairly good representation of their experience, but the caregivers’ opinion need to be considered.


Study design
A two-part mixed-study was carried out to provide a deeper understanding of caregivers' experiences [17]. The quantitative part was a cross-sectional single-center prospective study. The qualitative part was descriptive and comprehensive, using a phenomenological approach [18]. A convergent design where quantitative and qualitative data collection was simultaneous was used. The analysis of the two types of data was carried out separately. in the design, or conduct, or reporting, or dissemination plans of the research.

Participants and recruitment
The study was conducted in a medical oncology unit and its day hospital in a French tertiary hospital between February and May 2022. Patient-caregiver dyads were recruited on the basis of patients' visits to consultations or day hospitals. Caregivers were approached either by mail, telephone, or face-to-face. The inclusion criteria for patients were to be aged 18 years and older and to be diagnosed with digestive cancer. The inclusion criteria for caregivers were to be aged 18 years and over and to be designated as the primary caregiver by a patient with digestive cancer. Non-inclusion criteria were refusal to participate by any member of the dyad or inability to complete a questionnaire or participate in an interview (cognitive impairment, language barrier, reading difficulties). For all participants, sociodemographic variables were collected (age, gender, type of relationship, socio-professional category). For patients, their clinical situation (location, metastatic status, performance status (PS)) was extracted from medical records.

Quantitative data collection and analysis
The "Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) tool [19] guided the reporting in this study. A cross-sectional study based on two validated questionnaires was conducted with caregivers. The Caregiver Reaction Assessment (CRA) was used to measure the caregiver burden [20]. It was used in its validated French version [21], which includes 24 items structured into five burden domains: caregiver self-esteem (seven items), schedule burden (five items), lack of family support (five items), health burden (four items), and financial burden (three items). Caregivers responded using a five-point Likert scale (1 = strongly disagree to 5 = strongly agree). For each burden domain, a score was calculated. The Supportive Care Needs Survey for Partners & Caregivers (SCNS-PC) was used to identify the unmet supportive care needs (USCN) of caregivers [22]. We used its validated French version [23], which includes 41 items classified into four types of needs: health care service and information (18 items), emotional and psychological (16 items), work and social security (four items), and communication and family support (three items). Caregivers rated the need for help on a five-point scale that differentiates between no needs (1 = not applicable, 2 = fulfilled needs) and USCN (3 = low, 4 = moderate, 5 = high). We used the analysis method of the French team that validated the questionnaire, recoding answers 1 and 2 as 1 (no need) and responses 3 to 5 as 2 to 4. For each type of need, a score was calculated. A higher score meant more need for help.
Data were anonymized and descriptive statistics were performed to summarize responses in terms of frequencies, percentages, means, standard deviations (SDs), ranges, and medians, as appropriate.

Qualitative data collection and analysis
The Consolidated Criteria for Reporting Qualitative Research (COREQ) checklist [24] guided the reporting in this study. The patients and their caregivers participated in individual semi-structured interviews. The first author conducted the interviews, in the hospital for the patients and by telephone primarily for the caregivers. She was trained to conduct an interview beforehand during a simulation session with the last author trained in qualitative research. The focus groups were conducted in French, and no non-participants was present during the interview. Two semi-structured interview guides constructed from the literature were used, one for caregivers and one for patients (S1 File). They consisted of open-ended questions allowing the interviewee to express himself freely on the topic of caregiving for patients with digestive cancers. They addressed the same themes: physical and psychological state of the caregiver; impact on daily life and difficulties encountered or positive experiences lived; impact on the caregiver-patient relationship; vision of the future. The interviews were recorded (audio) and then transcribed and analyzed independently by the first and third authors. The qualitative analysis was then carried out by the first and third, using the six-step thematic analysis by Braun and Clarke [25]. Briefly, it consisted of categorization and thematization of all the verbatims from each group through systematic inductive coding. The authors compared their analyses until they reached a common interpretation, following four stages of analysis (immersion in the data, coding, creation of categories, and identification of themes). NVIVO V.11 software was used for coding. Data collection was continued until saturation was met, i.e. when no new categories appeared in the thematic analysis [26]. After anonymization, each dyad was assigned a number, and a letter was used to differentiate caregivers (C) and patients (P). This allowed the creation of an identification code (ID) for each participant.
The interviews with patients and caregivers were analyzed separately to consider the perspective of each. Then, each dyad was studied and compared one by one, to detect possible differences or similarities within the dyad.

Ethics statement
Informed consent was obtained from each patient and caregiver included. For the interviews, written consent was obtained. Ethical approval was granted by a local ethics committee (Groupe Nantais d'Ethique dans le Domaine de la Santé) on February 16, 2022 (#GNEDS20220216).

Quantitative results
The questionnaires were distributed to 63 caregivers. Thirty-two were returned, representing a response rate of 50.8%. The characteristics of the participants are described in Table 1.
The mean age of the caregivers was 56.1 years (SD, 19.0), and 71.9% were female. Most (81.3%) lived with the patient and 71.9% were their spouse. 93.8% of them reported providing emotional support, and 78.1% helping with household tasks. The majority (71.0%) were not working, either retired or not employed. The patients they cared for were mainly male (62.5%) with a mean age of 63.3 years (SD, 11.9). Most patients (71.9%) had a good PS (0-1).
According to SCNS-PC's responses, only two (6.3%) caregivers had no USCN, meaning that 93.7% of caregivers had at least one unmet need. On average, caregivers noted that 46.3% of the needs presented were unmet (19 of 41 needs items). Considering moderate to high USCN, 56.3% reported at least 10. Across the four domains of needs, the highest scores were found for healthcare service and information needs (mean, 2.0; SD, 0.8) followed by emotional and psychological needs (mean, 1.9; SD, 0.6). In third and fourth place were the needs related to family support and communication (mean, 1.6; SD, 0.9) and work and social security (mean, 1.5; SD, 0.6).
For each questionnaire, the responses to each item are presented in Figs 1 and 2.

Qualitative results
Of the 32 patient-caregiver dyads for which we had quantitative results, 10 gave their consent to participate in the interviews. The main reasons for declining the interviews were lack of time or because it seemed too intimate. The average duration of an interview was 35  min for caregivers and 30  min for patients. The characteristics of the participants are presented in Table 2. The median age was 60.5  years for caregivers and 67.5  years for patients. Eight caregivers and four patients were female. Seven caregivers were spouses. One caregiver did not live with the patient. Two caregivers and one patient were employed. Four patients had a PS � 2. The median duration of presence as a caregiver was 15  months.
The themes and subthemes, along with illustrative quotes from the caregiver and patient interviews are presented in Tables 3 and 4 respectively.
Quotes are identified by the participant's anonymizing ID. Additional quotes are reported in S2 File.
What is it like to be a caregiver? The caregiver's point of view. Illness is an upheaval in the caregiver's life. Illness suddenly thrusts loved ones into the role of caregiver. This role disrupts their habits, changes their daily life (C25), and has an impact on their organization. This ranges from the distribution of household tasks to putting their studies on hold (C54) and being off work. They take on new roles within their own families by having to take care of their siblings (C54) or children (C15) on their own. Their habits are affected by financial problems or administrative procedures considered a waste of time. They are also forced to review their plans, they can no longer plan in the long term and must live in the present (C53). All of this is the consequence of the fact that the patient's illness is now their major concern (C33). All their free time are devoted to the patient so they change their schedule, put things aside (C01) and organize themselves around the illness. One of the things standing out is their desire to be involved and informed, they are curious (C12) about cancer and its evolution. All of this leads caregivers to forget themselves and their health: "My own needs [. . .] I don't forget them, but I know how to put them in brackets for the time it takes" (C33). Finally, it weighs on them mentally and physically. They are drained (C06) and emotionally much sadder (C06). Because of the stress they often don't eat, they don't sleep (C15), so much so that they have to take pills, take naps during the day, or watch TV at night (C15, C26, C53). Sometimes they prefer to sleep alone in a room alone to sleep better (C53).
He feels alone and helpless dealing with the disease and suffers its consequences. The lack of control they have over the situation is difficult. Caregivers feel helpless in certain situations

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and do not know how to act. The main source of helplessness is pain, "when she really suffers [. . .] but I can't do anything" (C51). Another difficulty is the unknown (C06) because they are often unprepared to deal with the progression of cancer, which can be fatal. At the same time, they also feel alone because they deplore the lack of time given to them by medical staff, and sometimes have to cry to get information from doctors (C06), they also raise the issue of a true caregiver status (C33). The illness can even affect their relationship with the patient because they do fewer activities together and tensions can arise between them (C06). At the level of intimacy, chemo also has an impact on their sexuality.
Despite this, he naturally assumes his role while managing to remain positive. Despite this, caregivers naturally assume their role. For them, it is normal (C25) and is not considered a constraint (C01). For spouses, it is a role inherent to their marital status (C12). It is also a way of giving back to the patient (C01). On the other hand, caregivers can draw positive things from the situation because it changes their outlook on life (C25), they see things more positively. It can make them feel useful (C33) and more accomplished (C12).
What is it like to be a caregiver? The patient's point of view. The patient sees the caregiver take on his new role naturally and becoming closer to him. From the patient's perspective, taking on this role is not something forced on the caregiver (P26), because they are married (P06) or because it is in the caregiver's values to put others first (P33). The caregiver also seems to be closer to them, their relationship would be strengthened (P12) and they would communicate more (P15).
The caregiver becomes the anchor of the patient. With the diagnosis of cancer, the patient needs more attention and over time sees himself becoming the center of attention of the  caregiver. He sees that the caregiver is always worried about him (P25) and always wants to be with him: "She wants to go everywhere with me, if I don't forbid her to come, she comes. Even for one day of hospitalization, she comes." (P12). He sees how curious the caregiver is about his care because he asks many questions (P06) and sometimes more than the patient. The patient admits that he needs the caregiver, that he is indispensable to him (P26) because he does everything at home now (P15) and his presence in difficult moments is essential. In fact, the patient would not know what to do without the caregiver. They are grateful (P26) and even consider the caregiver as important as medical care (P33). But he notices that this disrupts the life of the caregiver. The patient notes that all of this is putting a strain on the caregiver. He sees that the caregiver is not sleeping, is losing weight  (P53). Emotionally, he sees that it makes the caregiver sad (P06). When the caregiver has to provide medical care to the patient, he knows how much it can cost the caregiver because he is afraid of hurting the patient (P33). In addition, he realizes that it also affects their work life. The caregiver does not express the difficulties he is experiencing but the patient is not fooled (P33), he sees the caregiver hiding them from him, whether it is his need for help or his emotions. The patient suspects a desire to protect him and not to worry him (P25). And this worries him, he feels guilty about the caregiver and would like to protect him. All this added up, the patient ends up worrying. He fears leaving the caregiver alone in case of a fatal outcome and laments that the caregiver sometimes forgets himself (P33). The patient then feels guilty and has the impression of being a burden (P15). Thus, he would like to lighten this burden and make the caregiver admit that he needs help (P15). The patient, therefore, tries to protect the caregiver in his way (P12) by hiding things about the disease (P12) or by making sure that the caregiver has as little to do as possible (P06).

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The differences and similarities of point of view between a patient and his caregiver. The results of the comparison of each dyad individually, along with illustrative quotes are presented in Table 5.
Quotes are only identified by a letter and not with participants' ID, to ensure no possible re-identification, given some of the topics discussed.
We consider similarities in the topics addressed in the same way by caregiver and patient regarding the experience of being a caregiver and differences when they express two real points of view that oppose each other. Thus, topics that are not common are not necessarily differences, some topics may not have been addressed by one of the dyad members.
For two dyads, we did not detect discrepancies. The main theme of the discrepancies detected for the other dyads concerned their relationship. For example, one patient felt that their relationship had improved, while the caregiver felt that it had grown apart. Another caregiver felt that the patient was not telling him everything, while the caregiver said that the patient was not hiding anything.
There were many themes on which the patient and caregiver of the same pair agreed, showing the patient's ability to correctly estimate the caregiver's experience, notably by considering the caregiver's burden.

Discussion
This mixed-method study gave a general picture of the experiences of caregivers of digestive cancer patients. It shows the complex impact of caring for a patient with digestive cancer on the caregiver, and the difference in vision that a patient can have on these consequences compared to his caregiver.
Disruption of schedule was noted as the greatest burden from CRA's responses (score = 3.3). The same trend was found for colorectal cancer caregivers in a study also using this questionnaire (score = 3.05) [27]. Other studies have shown the importance of this impact by other means than the CRA [28,29] as it appears also from our interviews. Several studies show that spousal caregivers report a greater burden on their schedule [30,31]. This can be related to family commitments such as childcare and social relationships exacerbating perceived burden and scheduling conflicts. Our caregiver population is predominantly spouses; this may explain the fact that this was the primary burden reported in our study. Financial and health impacts are noted in second and third position by caregivers, again following the same trend as the study cited above [27].
Based on SCNS-PC responses, their first need for help was for health care and information (score = 2.0). This is consistent with the literature, both in France (1.69) [32] and Germany (1.91) [33]. This corroborates what was declared by caregivers during the interviews: they need to be informed about everything concerning the patient and the disease. Lack of information is known to be a major source of stress for caregivers [34,35]. In our population, the proportion of caregivers with at least one USCN (93.7%) was higher than in the literature, where ranging from 16 to 68% [34,36] can be found. Our results are closer to the ones of Sklenarova et al, in which this score reached 85.6% [33]. The latter revealed that few variables were associated with caregivers' cancer-related USCNs, but that the number of patients' USCNs consistently predicted those of caregivers. Patient' USCN were not assessed in our study, which precludes the measurement of this correlation.
The positive aspects of caregiving are reflected in the CRA self-esteem dimension (score = 3.8), even if this score is slightly lower than the one in another study (4.51) [31]. Feelings of fulfillment and usefulness highlighted from the interviews are in tune with what is to be found in previous literature [3,10].

Differences in the topics addressed
The caregiver-patient relationship (Continued ) The comparison of themes between the interviews with patients and caregivers and the analysis of the pairs individually reveals a large number of similarities. This shows that the patients have a fairly good representation of what the caregiver is going through, both in terms of the disruption of their habits and the different burdens they may feel, even though caregivers do not express their needs and difficulties. Hiding one's difficulties to appear strong to the patient is a known phenomenon [3,37]. However, this reluctance of caregivers to express their feelings has previously been shown to harm them [38]. This may explain why, as reported in various studies, a significant proportion of patients may underestimate the burden and difficulties of their caregivers [10,39]. Discrepancies in opinion were also found in an American study, with patients underestimating the difficulty of the psychosocial aspects of caregiving [40]. This is an important issue since this underestimation may significantly be related to lower quality of life and higher levels of depression and anxiety of the caregiver [39], and as it is known to be an important determinant of caregiver well-being [41]. Because patients and caregivers can influence each other [42], it is important to get the patient's opinion on what his caregiver is experiencing, and to promote communication between them. This would make it possible to highlight the differences in viewpoints between them, and improve their respective qualities of life. The main discrepancy between patients and caregivers concerns the evolution of their relationship dynamics. In the themes, caregivers report a deterioration in their

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relationship while patients feel closer, and at the level of a pair, several couples report an evolution of their relationship in opposite directions. One study may partly explain this finding by suggesting that female caregivers, our predominant population, are more likely to describe themselves as grieving the relationship they previously shared with the patient [3]. Moreover, the fact that 80% of the caregivers interviewed were women and 60% of the patients were men could partly explain the differences in their points of view. According to Manne et al., a disparity between the views of patients and caregivers regarding their relationship is frequent [41]. In the literature, the results are also conflicting with studies reporting a deterioration [43] or an improvement in the relationship [3]. All this underlines the importance of supporting caregivers and identifying their psychosocial needs to be able to propose adjustments and direct them to the appropriate actors and structures, especially when the end of life approaches. In France, specific solutions exist (the leave for caregivers, the right to rest, etc.), but they are often ignored by caregivers [44]. Studies that have explored couple-based interventions demonstrated their benefit for both patient and caregiver [45,46]. For future research, it would be interesting to also investigate in more detail interventions based on parent/child and sibling relationships.
The principal strength of our study is its mixed-method approach. Some limitations were identified. Due to our limited sample size, additional data are needed for these results to be generalized. It would be of interest to submit the SCNS-PC and CRA questionnaires to the patients the same way we did with their caregiver, but it would mean having a psychometric validation of the questionnaires from their point of view. This may be an insightful work in the future. In addition, collecting data at different points in time would allow for an assessment of the evolution of experiences throughout the relationship. Indeed, it is known that the burden can evolve depending on the history of the disease [28].
Our study contributes to the growing literature in this area and shows that caregivers need as much support as patients. Our results are similar in many regards to other studies studying caregivers of patients with different types of cancer. This highlights the fact that caregivers' concerns are the same for many, despite populations with different characteristics and studies spread over time. Their consideration is not yet optimal. This study demonstrates the importance of considering both perspectives to better understand the caregiver's experience. Finally, it provides direction for implementing psychosocial interventions for the patient-caregiver dyad rather than interventions for caregivers or patients alone.